Abstract
Purpose
To define the prevalence and risk factors of anxiety and examine rates and predictors of psychotherapy and integrative medicine service use in breast cancer survivors on aromatase inhibitors (AIs).
Methods
Observational study of patients with histologically confirmed stage 0–III hormone receptor-positive breast cancer taking a third-generation AI at the time of enrollment. Patients completed self-report measures of anxiety and utilization of psychotherapy and integrative medicine services at a single time-point. We used multivariate logistic regression analyses to identify factors associated with anxiety and receipt of anxiety treatment services.
Results
Among the 1085 participants, the majority were younger than 65 years of age (n = 673, 62.0%) and white (n = 899, 82.9%). Approximately one-third (30.8%) reported elevated anxiety (≥ 8 on the anxiety subscale of the Hospital Anxiety and Depression Scale). Of patients with elevated anxiety, only 24.6% reported receiving psychological counseling, 25.3% used integrative medicine services, and 39.8% received either type of treatment since their diagnosis. Patients with an education level of high school or less were less likely to receive psychological counseling (AOR, 0.43, 95% CI 0.19–0.95) and integrative medicine services (OR 0.30, 95% CI 0.12–0.72) than patients with higher levels of education.
Conclusions
Anxiety is common in breast cancer patients treated with AIs yet the majority of anxious patients do not receive evidence-based treatment, even when these treatments are available. Better systematic anxiety screening and treatment initiation are needed to reduce disparities in care by education level.
Similar content being viewed by others
References
Howlader N, Noone AM, Krapcho M, Miller D, Brest A, Yu M et al (eds) (2018) SEER cancer statistics review, 1975–2016, National Cancer Institute. Based on November 2017 SEER data submission, posted to the SEER web site, April 2018
Surveillance, Epidemiology, and End Results (SEER) Program (http://www.seer.cancer.gov) Research data (1975–2016), National Cancer Institute, DCCPS. Surveillance research program, released April 2019, based on the November 2018 submission
Burstein HJ, Lacchetti C, Anderson H, Buchholz TA, Davidson NE, Gelmon KA, Giordano SH, Hudis CA, Solky AJ, Stearns V, Winer EP, Griggs JJ (2019) Adjuvant endocrine therapy for women with hormone receptor-positive breast cancer: ASCO Clinical Practice Guideline Focused Update. J Clin Oncol 37(5):423–438. https://doi.org/10.1200/jco.18.01160
Pagani O, Regan MM, Walley BA, Fleming GF, Colleoni M, Láng I, Gomez HL, Tondini C, Burstein HJ, Perez EA, Ciruelos E, Stearns V, Bonnefoi HR, Martino S, Geyer CE, Pinotti G, Puglisi F, Crivellari D, Ruhstaller T, Winer EP, Rabaglio-Poretti M, Maibach R, Ruepp B, Giobbie-Hurder A, Price KN, Bernhard J, Luo W, Ribi K, Viale G, Coates AS, Gelber RD, Goldhirsch A, Francis PA (2014) Adjuvant exemestane with ovarian suppression in premenopausal breast cancer. J Clin Oncol 371(2):107–118. https://doi.org/10.1056/NEJMoa1404037
Saha P, Regan MM, Pagani O, Francis PA, Walley BA, Ribi K, Bernhard J, Luo W, Gomez HL, Burstein HJ, Parmar V, Torres R, Stewart J, Bellet M, Perello A, Dane F, Moreira A, Vorobiof D, Nottage M, Price KN, Coates AS, Goldhirsch A, Gelber RD, Colleoni M, Fleming GF (2017) Treatment efficacy, adherence, and quality of life among women younger than 35 years in the International Breast Cancer Study Group TEXT and SOFT Adjuvant Endocrine Therapy Trials. J Clin Oncol 35(27):3113–3122. https://doi.org/10.1200/jco.2016.72.0946
Ryden L, Heibert Arnlind M, Vitols S, Hoistad M, Ahlgren J (2016) Aromatase inhibitors alone or sequentially combined with tamoxifen in postmenopausal early breast cancer compared with tamoxifen or placebo—meta-analyses on efficacy and adverse events based on randomized clinical trials. Breast 26:106–114. https://doi.org/10.1016/j.breast.2016.01.006
Goss PE, Ingle JN, Pritchard KI, Robert NJ, Muss H, Gralow J, Gelmon K, Whelan T, Strasser-Weippl K, Rubin S, Sturtz K, Wolff AC, Winer E, Hudis C, Stopeck A, Beck JT, Kaur JS, Whelan K, Tu D, Parulekar WR (2016) Extending aromatase-inhibitor adjuvant therapy to 10 years. NEJM 375(3):209–219. https://doi.org/10.1056/NEJMoa1604700
Gandubert C, Carriere I, Escot C, Soulier M, Hermes A, Boulet P, Ritchie K, Chaudieu I (2009) Onset and relapse of psychiatric disorders following early breast cancer: a case–control study. Psychooncology 18(10):1029–1037. https://doi.org/10.1002/pon.1469
Mayer M (2010) Lessons learned from the metastatic breast cancer community. Semin Oncol Nurs 26(3):195–202. https://doi.org/10.1016/j.soncn.2010.05.004
Tsaras K, Papathanasiou IV, Mitsi D, Veneti A, Kelesi M, Zyga S, Fradelos EC (2018) Assessment of depression and anxiety in breast cancer patients: prevalence and associated factors. Asian Pac J Cancer Prev 19(6):1661–1669. https://doi.org/10.22034/apjcp.2018.19.6.1661
Mehnert A, Koch U (2008) Psychological comorbidity and health-related quality of life and its association with awareness, utilization, and need for psychosocial support in a cancer register-based sample of long-term breast cancer survivors. J Psychosom Res 64(4):383–391. https://doi.org/10.1016/j.jpsychores.2007.12.005
Mehnert A, Brahler E, Faller H, Harter M, Keller M, Schulz H, Wegscheider K, Weis J, Boehncke A, Hund B, Reuter K, Richard M, Sehner S, Sommerfeldt S, Szalai C, Wittchen HU, Koch U (2014) Four-week prevalence of mental disorders in patients with cancer across major tumor entities. J Clin Oncol 32(31):3540–3546. https://doi.org/10.1200/jco.2014.56.0086
Haskins CB, McDowell BD, Carnahan RM, Fiedorowicz JG, Wallace RB, Smith BJ, Chrischilles EA (2019) Impact of preexisting mental illness on breast cancer endocrine therapy adherence. Breast Cancer Res Treat 174(1):197–208. https://doi.org/10.1007/s10549-018-5050-1
Smith KL, Yeruva SLH, Blackford A, Huang CY, Westbrook KE, Harding BA, Smith A, Fetting J, Wolff AC, Jelovac D, Miller RS, Connolly R, Armstrong D, Nunes R, Visvanathan K, Stearns V (2018) Predictors of adherence to adjuvant endocrine therapy (ET) for early breast cancer (BC) in a prospective clinic-based cohort. Cancer Res 78(4). https://doi.org/10.1158/15387445.SABCS17-P3-12-02
Bender CM, Gentry AL, Brufsky AM, Casillo FE, Cohen SM, Dailey MM, Donovan HS, Dunbar-Jacob J, Jankowitz RC, Rosenzweig MQ, Sherwood PR, Sereika SM (2014) Influence of patient and treatment factors on adherence to adjuvant endocrine therapy in breast cancer. Oncol Nurs Forum 41(3):274–285. https://doi.org/10.1188/14.onf.274-285
Faller H, Strahl A, Richard M, Niehues C, Meng K (2017) Symptoms of depression and anxiety as predictors of physical functioning in breast cancer patients. A prospective study using path analysis. Acta Oncol 56(12):1677–1681. https://doi.org/10.1080/0284186x.2017.1333630
Merriman JD, Sereika SM, Brufsky AM, McAuliffe PF, McGuire KP, Myers JS, Phillips ML, Ryan CM, Gentry AL, Jones LD, Bender CM (2017) Trajectories of self-reported cognitive function in postmenopausal women during adjuvant systemic therapy for breast cancer. Psycho-oncology 26(1):44–52. https://doi.org/10.1002/pon.4009
Lidgren M, Wilking N, Jönsson B, Rehnberg C (2007) Health related quality of life in different states of breast cancer. Qual Life Res 16(6):1073–1081. https://doi.org/10.1007/s11136-007-9202-8
Chow S, Wan BA, Pidduck W, Zhang L, DeAngelis C, Chan S, Yee C, Drost L, Leung E, Sousa P, Lewis D, Lam H, Chow R, Lock M, Chow E (2019) Symptoms predictive of overall quality of life using the Edmonton Symptom Assessment Scale in breast cancer patients receiving radiotherapy. Clin Breast Cancer 19(6):405–410. https://doi.org/10.1016/j.clbc.2019.05.007
Sun H, Huang H, Ji S, Chen X, Xu Y, Zhu F, Wu J (2019) The efficacy of cognitive behavioral therapy to treat depression and anxiety and improve quality of life among early-stage breast cancer patients. Integr Cancer Ther. https://doi.org/10.1177/1534735419829573
Ye M, Du K, Zhou J, Zhou Q, Shou M, Hu B, Jiang P, Dong N, He L, Liang S, Yu C, Zhang J, Ding Z, Liu Z (2018) A meta-analysis of the efficacy of cognitive behavior therapy on quality of life and psychological health of breast cancer survivors and patients. Psycho-oncology 27(7):1695–1703. https://doi.org/10.1002/pon.4687
Andersen BL, DeRubeis RJ, Berman BS, Gruman J, Champion VL, Massie MJ, Holland JC, Partridge AH, Bak K, Somerfield MR, Rowland JH (2014) Screening, assessment, and care of anxiety and depressive symptoms in adults with cancer: an American Society of Clinical Oncology guideline adaptation. J Clin Oncol 32(15):1605–1619. https://doi.org/10.1200/jco.2013.52.4611
Lengacher CA, Johnson-Mallard V, Post-White J, Moscoso MS, Jacobsen PB, Klein TW, Widen RH, Fitzgerald SG, Shelton MM, Barta M, Goodman M, Cox CE, Kip KE (2009) Randomized controlled trial of mindfulness-based stress reduction (MBSR) for survivors of breast cancer. Psycho-Oncology 18(12):1261–1272. https://doi.org/10.1002/pon.1529
Wurtzen H, Dalton SO, Elsass P, Sumbundu AD, Steding-Jensen M, Karlsen RV, Andersen KK, Flyger HL, Pedersen AE, Johansen C (2013) Mindfulness significantly reduces self-reported levels of anxiety and depression: results of a randomised controlled trial among 336 Danish women treated for stage I–III breast cancer. Eur J Cancer 49(6):1365–1373. https://doi.org/10.1016/j.ejca.2012.10.030
Greenlee H, DuPont-Reyes MJ, Balneaves LG, Carlson LE, Cohen MR, Deng G, Johnson JA, Mumber M, Seely D, Zick SM, Boyce LM, Tripathy D (2017) Clinical practice guidelines on the evidence-based use of integrative therapies during and after breast cancer treatment. CA Cancer J Clin 67(3):194–232. https://doi.org/10.3322/caac.21397
Lyman GH, Greenlee H, Bohlke K, Bao T, DeMichele AM, Deng GE, Fouladbakhsh JM, Gil B, Hershman DL, Mansfield S, Mussallem DM, Mustian KM, Price E, Rafte S, Cohen L (2018) Integrative therapies during and after breast cancer treatment: ASCO endorsement of the SIO clinical practice guideline. J Clin Oncol 36(25):2647–2655. https://doi.org/10.1200/jco.2018.79.2721
Thekdi SM, Trinidad A, Roth A (2014) Psychopharmacology in cancer. Curr Psychiatry Rep 17(1):529. https://doi.org/10.1007/s11920-014-0529-x
Hopwood P, Howell A, Maguire P (1991) Screening for psychiatric morbidity in patients with advanced breast cancer: validation of two self-report questionnaires. Br J Cancer 64(2):353–356
Polanski J, Chabowski M, Chudiak A, Uchmanowicz B, Janczak D, Rosinczuk J, Mazur G (2018) Intensity of anxiety and depression in patients with lung cancer in relation to quality of life. Adv Exp Med Biol 1023:29–36. https://doi.org/10.1007/5584_2017_50
Jung JY, Lee JM, Kim MS, Shim YM, Zo JI, Yun YH (2017) Comparison of fatigue, depression, and anxiety as factors affecting posttreatment health-related quality of life in lung cancer survivors. Psychooncology. https://doi.org/10.1002/pon.4513
Deimling GT, Kahana B, Bowman KF, Schaeffer ML (2002) Cancer survivorship and psychological distress in later life. Psycho-Oncology 11(6):479–494. https://doi.org/10.1002/pon.614
Greer JA, Solis JM, Temel JS, Lennes IT, Prigerson HG, Maciejewski PK, Pirl WF (2011) Anxiety disorders in long-term survivors of adult cancers. Psychosomatics 52(5):417–423. https://doi.org/10.1016/j.psym.2011.01.014
Moadel A, Kolidas E, Ghavamian R (2016) Psychosocial needs assessment of underserved prostate cancer patients: survivorship program planning. J Clin Oncol 34(15_suppl):10107
Mosher CE, DuHamel KN (2012) An examination of distress, sleep, and fatigue in metastatic breast cancer patients. Psycho-Oncology 21(1):100–107. https://doi.org/10.1002/pon.1873
Hughes KL, Sargeant H, Hawkes AL (2011) Acceptability of the distress thermometer and problem list to community-based telephone cancer helpline operators, and to cancer patients and carers. BMC Cancer 11(46). https://doi.org/10.1186/1471-2407-11-46
Verdonck-De Leeuw I, Krebber AM, Cuijpers P, De Bree R, Leemans CR (2013) Benefits and costs of screening in clinical practice to identify head and neck cancer patients with untreated psychological distress after treatment. Psycho-Oncology 22:49. https://doi.org/10.1111/j.1099-1611.2013.3393
Burgoyne MJ, Bingen K, Leuck J, Dasgupta M, Ryan P, Hoffmann RG (2015) Cancer-related distress in young adults compared to middle-aged and senior adults. J Adolesc Young Adult Oncol 4(2):56–63. https://doi.org/10.1089/jayao.2014.0005
Rose JH, O’Toole EE, Einstadter D, Love TE, Shenko CA, Dawson NV (2008) Patient age, well-being, perspectives, and care practices in the early treatment phase for late-stage cancer. J Gerontol A Biol Sci Med Sci 63(9):960–968
Linden W, Vodermaier A, Mackenzie R, Greig D (2012) Anxiety and depression after cancer diagnosis: prevalence rates by cancer type, gender, and age. J Affect Disord 141(2–3):343–351. https://doi.org/10.1016/j.jad.2012.03.025
Jensen RE, Potosky AL, Moinpour CM, Lobo T, Cella D, Hahn EA, Thissen D, Smith AW, Ahn J, Luta G, Reeve BB (2017) United States population-based estimates of patient-reported outcomes measurement information system symptom and functional status reference values for individuals with cancer. J Clin Oncol 35(17):1913–1920. https://doi.org/10.1200/jco.2016.71.4410
Alcala HE (2014) Differential mental health impact of cancer across racial/ethnic groups: findings from a population-based study in California. BMC Public Health 14:930. https://doi.org/10.1186/1471-2458-14-930
Apenteng BA, Hansen AR, Opoku ST, Mase WA (2016) Racial disparities in emotional distress among cancer survivors: insights from the Health Information National Trends Survey (HINTS). J Cancer Educ 32(3):556–565. https://doi.org/10.1007/s13187-016-0984-7
Grassi L, Caruso R, Sabato S, Massarenti S, Nanni MG, the UniFe Psychiatry Working Group Coauthors (2015) Psychosocial screening and assessment in oncology and palliative care settings. Front Psychol 5(1485). https://doi.org/10.3389/fpsyg.2014.01485
Pachana NA, Byrne GJ, Siddle H, Koloski N, Harley E, Arnold E (2007) Development and validation of the Geriatric Anxiety Inventory. Int Psychogeriatr 19(1):103–114. https://doi.org/10.1017/s1041610206003504
Brown LF, Kroenke K, Theobald DE, Wu J, Tu W (2010) The association of depression and anxiety with health-related quality of life in cancer patients with depression and/or pain. Psychooncology 19(7):734–741. https://doi.org/10.1002/pon.1627
Wilson KG, Chochinov HM, Skirko MG, Allard P, Chary S, Gagnon PR, Macmillan K, De Luca M, O’Shea F, Kuhl D, Fainsinger RL, Clinch JJ (2007) Depression and anxiety disorders in palliative cancer care. J Pain Symptom Manag 33(2):118–129. https://doi.org/10.1016/j.jpainsymman.2006.07.016
Xiao F, Song X, Chen Q, Dai Y, Xu R, Qiu C, Guo Q (2017) Effectiveness of psychological interventions on depression in patients after breast cancer surgery: a meta-analysis of randomized controlled trials. Clin Breast Cancer 17(3):171–179. https://doi.org/10.1016/j.clbc.2016.11.003
Schellekens MPJ, van den Hurk DGM, Prins JB, Donders ART, Molema J, Dekhuijzen R, van der Drift MA, Speckens AEM (2017) Mindfulness-based stress reduction added to care as usual for lung cancer patients and/or their partners: a multicentre randomized controlled trial. Psycho-oncology 26(12):2118–2126. https://doi.org/10.1002/pon.4430
Bisseling EM, Schellekens MPJ, Jansen ETM, van Laarhoven HWM, Prins JB, Speckens AEM (2017) Mindfulness-based stress reduction for breast cancer patients: a mixed method study on what patients experience as a suitable stage to participate. Support Care Cancer 25(10):3067–3074. https://doi.org/10.1007/s00520-017-3714-8
Kenne Sarenmalm E, Mårtensson LB, Andersson BA, Karlsson P, Bergh I (2017) Mindfulness and its efficacy for psychological and biological responses in women with breast cancer. Cancer Med 6(5):1108–1122. https://doi.org/10.1002/cam4.1052
Carlson LE, Angen M, Cullum J, Goodey E, Koopmans J, Lamont L, MacRae JH, Martin M, Pelletier G, Robinson J, Simpson JS, Speca M, Tillotson L, Bultz BD (2004) High levels of untreated distress and fatigue in cancer patients. Br J Cancer 90(12):2297–2304. https://doi.org/10.1038/sj.bjc.6601887
Horneber M, Bueschel G, Dennert G, Less D, Ritter E, Zwahlen M (2012) How many cancer patients use complementary and alternative medicine: a systematic review and meta-analysis. Integr Cancer Ther 11(3):187–203. https://doi.org/10.1177/1534735411423920
Link AR, Gammon MD, Jacobson JS, Abrahamson P, Bradshaw PT, Terry MB, Teitelbaum S, Neugut A, Greenlee H (2013) Use of self-care and practitioner-based forms of complementary and alternative medicine before and after a diagnosis of breast cancer. Evid Based Complement Altern Med. https://doi.org/10.1155/2013/301549
Greenlee H, Kwan ML, Ergas IJ, Sherman KJ, Krathwohl SE, Bonnell C, Lee MM, Kushi LH (2009) Complementary and alternative therapy use before and after breast cancer diagnosis: the Pathways Study. Breast Cancer Res Treat 117(3):653–665. https://doi.org/10.1007/s10549-009-0315-3
Winter RW, Korzenik JR (2017) The practical pros and cons of complementary and alternative medicine in practice: integrating complementary and alternative medicine into clinical care. Gastroenterol Clin N Am 46(4):907–916. https://doi.org/10.1016/j.gtc.2017.08.013
Nahin RL, Barnes PM, Stussman BJ (2016) Insurance coverage for complementary health approaches among adult users: United States, 2002 and 2012. NCHS Data Brief 235:1–8
Funding
This research is funded in part by Grants from the National Cancer Institute/National Institutes of Health (R01 CA158243, P30-CA008748), and the Translational Research and Integrative Medicine Fund at the Memorial Sloan Kettering Cancer Center, and the National Institute on Aging/National Institutes of Health and American Federation for Aging Research (Trevino, K23AG048632). The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding agencies.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Dr. Iyengar reported receiving personal fees from Novartis outside the submitted work. All other authors have no conflicts of interest to disclose.
Ethical approval
All procedures performed in this study were in accordance with the ethical standards of the institutional review board of participating institutions and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Data archive
Dr. Jun J. Mao has full control of all primary data and agrees to allow the journal to review the data if requested.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Trevino, K.M., Iyengar, N., Li, Q. et al. Receipt of psychological counseling and integrative medicine services among breast cancer survivors with anxiety. Breast Cancer Res Treat 184, 301–310 (2020). https://doi.org/10.1007/s10549-020-05859-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10549-020-05859-0